Background. Complete anatomic knowledge including all variations of the inferior laryngeal nerve (ILN) is mandatory forthyroid surgeon. Extralaryngeal terminal division (ETD) of the ILN has significant importance for the safety of thyroidectomy.Material and Methods. Surgical dissection of 200 ILNs was performed on 100 cases. The presence of ETD of the nerve wasdetermined intraoperatively. We propose by a surgical point of view a regional (segmental) classification of ETD of the ILN alongits cervical course. Results. ETD has been observed in 54/200 nerves (27%). Great majority are bifurcated nerves (trifurcation2%). Four types of ETD are classified. In type 1 (arterial; 46.3%), ETD has occurred near inferior thyroid artery (ITA). Intype 2 (postarterial; 31.5%), division has been found on postarterial segment. In type 3 (prelaryngeal; 11%), division has beenlocated very close to laryngeal entry point. In type 4 (prearterial; 11%), ETD has occurred before the nerve crossing the ITA.Conclusions. ETD of the ILN is a common anatomical variation. The bifurcation occurs in the ILN at various distances fromlaryngeal entry point.The classification increasing surgeons’ awarenessmay help to simplify identification and exposure of terminalbranches. Preservation of both extralaryngeal terminal branches of the ILN has paramount importance for the safety of thyroidoperations.
1. Introduction
The safety of thyroid operations mainly depends on completeanatomic knowledge of the inferior laryngeal nerve (ILN)including all its variations. The nerve has many anatomicvariations along its expected and unexpected cervical course.The important one is cervical (extralaryngeal) branchingof the nerve. The presence of many branches and sensoryinnervations of adjacent tissues by thin branches of ILNhas been reported up to 90%. These branches have beenestablished by anatomical studies under direct ormicroscopicobservation [1, 2].These thin neural structures are not gener-ally perceived during surgery of the thyroid. Therefore, thesebranches are important scientific knowledge by anatomicalpoint of view but not by surgical point. On the other hand,extralaryngeal terminal division (bifurcation) of the ILN is
an anatomic variation macroscopically discovered duringoperations along cervical course of the nerve. The terminallybifurcated nerve has usually two larger branches which havesame or closer size as diameter. Larger branches of thenerve may have significant effect on function of laryngealmusculature. The thyroid surgeon must carefully expose andpreserve the integrity of both terminal branches if present.Therefore, macroscopic terminal division of the nerve seemsto carry great importance by surgical point of view.
In this study, we aim to establish the rate of anatomicalfeatures and location of division along cervical course ofthe nerve and surgical importance of extralaryngeal terminalbifurcation of the ILN in series of thyroidectomy cases. Wetry to classify anatomical location of division point on thecervical course of the nerve.
2 Journal of Thyroid Research
2. Patients and Methods
A prospective study on surgical anatomy of the ILN was con-ducted on 100 patients with surgical diseases of the thyroidgland between May 2009 and September 2012. Patients withreoperative surgery for treatment of recurrent diseases werenot included. Total thyroidectomy is the surgical procedurein all these 100 patients. All operations were performed bya single surgeon in order to provide a standard dissection.Main subjects of this study are the presence and incidenceof extralaryngeal terminal division of the nerve which aremacroscopically observed. Location of this division alongcervical course of the ILN is determined. Lateral sides(unilaterally right or left, or bilateral) of the terminal divisionare also noted during thyroid operations.
2.1. The Dissection Technique of ILN. After freeing andmedially mobilizing lateral lobes of the thyroid gland at bothsides with classical surgical approach, the inferior thyroidarteries (ITA) were identified, isolated, and a loop of silksuture was placed around arteries for traction. With usuallateral approach, ILNs were identified below the artery andfully isolated at both sides. The nerve is carefully exposedin the trachea-esophageal groove until its laryngeal entrypoint. The dissection is performed using binocular loupe. Ifmacroscopically and clearly delineated terminal divisions ofthe nerve are identified along its cervical course, we studyanatomical features of these branches.
2.2. Extralaryngeal Terminal Division of the ILN. Division ofthe ILN occurs along its cervical course prior to laryngealentry. The branches are macroscopically observed duringthyroid operations, and they enter separately into the larynxby different points.
2.3. Classification of Terminal Division of the Nerve. We pro-pose a regional (segmental) classification of extralaryngealterminal division of the ILN along its cervical course. Theclassification is based on surgical exposition steps of theentire nerve and on the rate of different location of thebifurcation point. Risk regions for injury to the nerve arealso taken into account for classification of extralaryngealbifurcation of the ILN by surgical point of view. Regions andanatomical location of terminal division is classified basingon two relatively constant landmarks; the neurovascular (ILNand ITA) crossing point and laryngeal entry point of thenerve (Table 1; Figure 1).
3. Results
Results were obtained from surgical dissection of 100 con-secutive total thyroidectomy cases. Two hundred ILNs wereidentified, isolated, and entirely exposed along their cervicalcourses until the laryngeal entry. Seventy-seven percent ofour patients are females.The incidence and anatomic featuresof extralaryngeal terminal division of the ILN are the mainsubject of the study.
Table 1: Classification of anatomical location of terminal divisionpoint of the ILN∗.
Type Region Definition
1 ArterialDivision occurs at or closely adjacent (±5mm) to neurovascular crossing of the
ILN and the ITA∗.
2 PostarterialDivision occurs in the first (proximal)
half of the distance betweenneurovascular crossing and laryngeal
entry point of the ILN.
3 PrelaryngealDivision occurs in the second (distal) halfof the distance between neurovascularcrossing and laryngeal entry point of the
ILN.
4 PrearterialDivision occurs before (proximal to)neurovascular crossing of the ILN and
the ITA.∗ILN: inferior laryngeal nerve. ITA: inferior thyroid artery.
Extralaryngeal terminal divisions of ILNs were deter-mined in 43 (43%) patients. We observed bilateral division in11 (11%) patients. Extralaryngeal terminal division has beenmacroscopically observed in 54/200 nerves (27%). The rateof division of the ILN is 19% and 35% at right and left sides,respectively (Table 2).
The ILNs have been terminally trifurcated (divided by3 branches) along their cervical courses in 4 (4%) patientsunilaterally, 2 trifurcations at right or left sides each. Thisresult reflects an incidence of trifurcation as 2% of exposedILNs (Table 2; Figure 2).
The location of terminal division along cervical courseof the nerve is another remarkable finding of the presentstudy. The cervical course of the nerve is divided by foursegments in which the neuro-vascular crossing (the ILN andthe ITA) and laryngeal entry points are found as importantlandmarks for regional classification and location of terminaldivision of the nerve. Approximately half (46.3%) of theterminal division of the ILN has occurred in arterial region.Type 1 is a more common location of division point followedby Type 2. Type 3 (prelaryngeal) and Type 4 (prearterial)have seldom observed as location of terminal division of theILN (Table 3). Intraoperative photos of various locations ofterminal division point of the ILN show in vivo anatomicvariations of the nerves (Figures 3, 4, 5, and 6).
4. Discussion
Microanatomic studies have shown that the ILN dividesintralaryngeal branches to anastomose with branches of theinternal laryngeal nerve. Size of these branches has beenreported 0.6mm as diameter [3]. When a surgeon macro-scopically observes a single trunk nerve in its cervical course,it has intralaryngeal branches for connections of laryngealnerves. Sometimes these branches have been exposed priorto laryngeal entry. Therefore, we can comment that extrala-ryngeal terminal division of the ILN is a premature branchingof the nerve. By a surgical point of view, the awareness about
Journal of Thyroid Research 3
The thyroid
Laryngeal entryILN
Prelaryngeal
ILN Postarterial
Prearterial Arterial
Inferior thyroid artery
10 mm
Figure 1: Segments in cervical course of the inferior laryngeal nerve (ILN).
Table 2: The rate and lateral site of terminal division (bifurcation) of the inferior laryngeal nerve.
Cases Division Bilateral division Division at right side Division at left sideTotal thyroidectomy 100 43 (43)∗ 11 8 24Inferior laryngeal nerve
Trifurcation 200 54 (27)4 (2)
19 (19)2 (2)
35 (35)2 (2)
Sex (Female/male) 77/23 33/10 15/4 27/8∗Numbers in parentheses are percentages.
Figure 2: Extralaryngeal terminal trifurcation of the right ILN.Division of the nerve occurs at neurovascular crossing. ∗Anteriorbranch, ∗∗Posterior branch.
the occurrence of premature terminal division is importantthat exposing bifurcation and larger branches of the nerveseparately prevent nerve injury during thyroid operations. Inthis study, we try to increase surgeons’ awareness about thisanatomic variation of the ILN by anatomically classifying thedistribution of branching in its cervical course.
Complete exposure of ILN is mandatory to avoid nerveinjury and laryngeal muscle palsy. Its anatomic variationsthreaten nerve integrity even in experienced hands. Our
Figure 3: Terminal division of the left inferior laryngeal nerve (ILN)occurs at arterial segment (Type 1). ∗Anterior branch. ∗∗Posteriorbranch. ITA: inferior thyroid artery.
rates (27% of ILNs) of macroscopically discovered extrala-ryngeal terminal division show that this is a commonanatomic variation.Therefore, surgeons frequently encounterbifurcated nerve during thyroidectomy operations. Previousmanuscripts have also reported the usualness of this variation[1, 2, 4, 5]. The incidence of bifurcated nerve has beenreported between 18% and 43% [6–11]. Sometimes, we can
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Table 3: The incidence of terminal division of the ILN according to anatomical classification.
Type Regions Definition Right Left Total1 Arterial Division occurs at or closely adjacent to neurovascular crossing. 9 (47.4)∗ 16 (45.7) 25 (46.3)
2 Postarterial Division occurs in the first (proximal) half of the distance betweenneurovascular crossing and laryngeal entry. 7 (36.8) 10 (28.6) 17 (31.5)
3 Prelaryngeal Division occurs in the second (distal) half of the distance betweenneurovascular crossing and laryngeal entry. 2 (10.5) 4 (11.4) 6 (11.1)
Figure 4: Terminal division of the left inferior laryngeal nerve(ILN) occurs at post-arterial segment (Type 2). ∗Anterior branch.∗∗Posterior branch. ITA: inferior thyroid artery.
Figure 5: Terminal division of the left inferior laryngeal nerve(ILN) occurs at pre-laryngeal segment (Type 3). ∗Anterior branch.∗∗Posterior branch. ITA: inferior thyroid artery.
unusually find three terminal branches of the ILN in its cer-vical course. Our incidence (2% of ILNs) of trifurcated nerveshows that ILN is rarely divided three terminal branchesprior to its laryngeal entry. The mean incidence of terminaltrifurcation of the ILN has also been reported approximately2% (between 1% and 3.8%) in previous studies [6, 8, 10, 12].The incidence of extralaryngeal terminal division of the ILNis high in which surgeons must strongly take into account thepresence of this variation and be cautious exposing the ILN.
Figure 6: Terminal division of the left inferior laryngeal nerve(ILN) occurs at pre-arterial segment (Type 4). ∗Anterior branch.∗∗Posterior branch. ITA: inferior thyroid artery.
Terminal division of the nerve may occur unilaterallyor bilaterally at both sides. We generally observed unilateralbifurcation of the ILN in which 75% of our patients havegot unilateral variation. Bilateral terminal division of theILN is relatively uncommon. Bilaterality of this variationhas been observed in 11% of our thyroidectomy cases andin 25% of patients with bifurcated nerves. Extralaryngealbilateral division of the nerve has been reported in a largerange of incidence between 3, to 33% [6, 7, 9–11, 13]. Inour series, the left ILN (35%) is more commonly bifurcatedthan the right one (19%). The report of Makay et al. [12]confirms this finding of higher rate at the left side. Basedon anatomical knowledge, this is an expected result. Theleft nerve recurrent under aortic arch is longer than theright one which is recurrent under right subclavian artery.Therefore, extralaryngeal division of the longer nerve is morecommonly expected than the shorter one. On the otherhand, the majority of previous studies have reported equalor slightly higher incidence at the right side. The rate hasbeen found as 23, to 59% at the right and 10, to 49% at theleft side [6, 7, 9–11, 13]. Branched ILNs may represent a riskfactor for nerve palsy. Knowledge of this anatomical variationand its routine investigation are essential. Surgeon’s awarenessof bifurcated ILN at both sides is required for the safety ofthyroid operations.
In case of bifurcated ILN, anatomical location of divisionpoint along its cervical course is crucial in order to securely
Journal of Thyroid Research 5
identify, to properly expose all branches of the nerve, and toprotect nerve integrity without inadvertent injury to neuralstructures. In our study, we determined various locations ofdivision point along the cervical course of the exposed ILN.Approximately in half (25/54) of the bifurcated nerves, thedivision occurs at or very close to nerve-artery crossing point.Bifurcation of the nerve just adjacent to neuro-vascular (theILN and the ITA) crossing is the most common location ofthe division point of the ILN.The division of the nerve occursdistal to the ITA (after nerve-artery crossing) in approxi-mately 1/3 of our cases in which this is found as the secondcommon location along the cervical course of the nerve.Beside these two common findings, we also determined twoother locations of the division point. The bifurcation of thenerve seldom occurs proximal to the ITA (before nerve-artery crossing).The division point is uncommonly observedvery close to the laryngeal entry of the nerve.
We try to classify anatomic location of division pointof the ILN along its cervical course aiming to increasesurgeon’s awareness. In order to establish an understandableclassification some anatomic structures and surgical variablesare taken into account.
(1) Landmarks to delineate cervical segments along cer-vical course of the ILN: two relatively constant land-marks (inferior thyroid artery and laryngeal entrypoint) help to divide cervical course of the nerve byfour segments; pre-arterial, arterial, post-arterial, andpre-laryngeal.
(2) Surgical technique to identify and expose the ILN:the ILN is identified at close proximity of ITA bystandard lateral approach technique. The nerve dis-section begins in arterial region, and is proximallyand distally advanced towards laryngeal entry inorder to expose the entire nerve.
(3) Rates of division of the nerve in various locations:approximately half of nerve bifurcation occurs nearITA.
Therefore, anatomic landmarks, surgical technique ofnerve identification and exposition, and location rates ofdivision point contribute to the classification of extrala-ryngeal bifurcation. Extralaryngeal bifurcation of the ILNis a common variation which carries great importance forpreservation of its motor function. We think that to befamiliar with location of division point of the nerve in itscervical course is significantly helpful to avoid nerve injury.We propose an anatomical classification of extralaryngealterminal division of the ILN. Terminal division of the nerveis classified by four types.
Type 1. Thebifurcation occurs at or very close (−/+ 5mm) tonerve-artery crossing point.The identification and dissectionof the nerve generally begins at this point by standard lateralapproach. In experienced hands, the nerve is easily foundadjacent to the artery. Therefore, this type of bifurcation isalso easily identifiable with careful dissection. This locationis the most common type of nerve division in our series.
Both branches are individually followed until their separatedlaryngeal entry.
Type 2. After identification of the nerve trunk, the dissectionis advanced in both distal and proximal direction in order todisplay entire cervical course of the ILN. In some patients,nerve bifurcation occurs distally to the artery, near Berryligament. In our series, the rate of post-arterial (Type 2)division of the nerve is found approximately in one third ofour patients with bifurcated nerve.
Type 3. During distal dissection of the ILN trunk, anothertype of bifurcation is discovered at the most distal part ofthe extralaryngeal ILN. Pre-laryngeal (Type 3) bifurcationoccurs most distally just before laryngeal entry of the nerve.This distal part is generally covered by ligament of Berryand thyroidal tissue. This region where the nerve is moresuperficial is reported as the most dangerous site for nerveinjury. If the bifurcation is not identified proximally (Types1 and 2), surgeons are faced with a dangerous situation.Surgeons must be aware of this distal division of the ILN. Ifsurgeons identify single trunk of the nerve at arterial region,the dissection is carefully advanced to distal part for possiblepre-laryngeal bifurcation.This type of most distal bifurcationmust take a strong place in surgeons mind in order to avoid adisaster after the operation. Fortunately, pre-laryngeal (Type3) division of the nerve seldom occurs as 11% of our patientswith bifurcated nerve.
Type 4. Thedissection of the nerve is also advanced proximalto the artery along cervical course of the ILN. In somepatients, bifurcation of the nerve is found at proximal seg-ment of the nerve before artery crossing. Pre-arterial (Type 4)bifurcationwhich is found in 11%of our patients, is a relativelyuncommon variation according to Types 1 and 2 division.
In case of bifurcation of the ILN, the location of motorfibers in nerve branches has extreme importance for preser-vation motor function. The motor fibers are located exclu-sively in the anterior branch, and the posterior branch issensory in function [4, 7, 9, 11]. In some cases. posteriorcricoarytenoid (PCA) muscles receive any kind of nervefibers from posterior division of the ILN. These fibers con-tribute innervations of PCA muscle [14, 15]. On the otherhand, Maranillo et al. [16] have reported that PCA muscles,the only abductor muscle of the larynx receive motor fiberfrom anterior division of the ILN.
Extralaryngeal terminal branches of the ILN can bea potential cause of nerve injury due to visual misiden-tification. This anatomical variation cannot be predictedpreoperatively and might be associated with higher rateof nerve injury [17]. Extralaryngeal bifurcation of the ILNincreases the risk of vocal cord palsy by two folds [18].Recognition of bifurcation is crucial. Preservation of allbranches is required for prevention of vocal cord palsy. Wethink that the most dangerous situation is misidentificationand misinterpretation of relatively larger posterior branch asthe main trunk of the nerve. In this situation, the anteriorbranch is under the greatest risk. Inadvertent division ofmotor fibers may lead to laryngeal muscles palsy despite the
6 Journal of Thyroid Research
surgeon believing the nerve was preserved. In recent yearsintraoperative neural monitoring (IONM) assessing motorfunction of the nerve, helps surgeons to identify securely theILN during thyroid surgery. IONM has gained widespreadacceptance as an adjunct to visual nerve identification. Visualidentification and a standard and uniform use of IONMfacilitate to establish motor fibers of the nerve especially inhigh risk patients [19, 20]. Anatomical variations of the nerveincluding extralaryngeal divisionmight be considered as highrisk situations. Therefore, visual identification of the ILNand IONM may be extremely helpful for preserving motorfunction and preventing vocal cord palsy in case of bifurcatedILN.
5. Conclusion
Extralaryngeal terminal division of the ILN is a commonanatomical variation.
The bifurcation occurs in different segment of the ILNalong its cervical course at various distances from cricothy-roid membrane (laryngeal entry point). In the majority ofsuch cases, the point of division is located near arterialjunction (ILN and ITA crossing point). On the other hand,surgeons must take into account that there are also uncom-mon locations of the bifurcation.
The anatomic classification of division pointmay increasesurgeons’ awareness of this variation. The classification mayalso lead to simplify identification and exposure of terminalbranches.
The ILN must be macroscopically identified and pre-served during thyroidectomy in order to prevent vocalcord palsy. Identification, exposure, and preservation ofboth extralaryngeal terminal branches of the ILN possessparamount importance in order to prevent nerve injury.Misidentification and misinterpretation of the posteriorbranch as the main trunk of the ILN put the anterior branchandmotor fibers under the greatest risk. Inadvertent divisionof motor fibers may lead to laryngeal muscles palsy despitethe surgeon believing the nerve was preserved.
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